2. Gibbon Systematics

It is generally accepted that gibbons, the great
apes and humans together form the monophyletic group Hominoidea (Groves, 1989). It
has also been widely accepted in recent years that the gibbons constitute the sister
group to the great apes and humans (Fig. 1) and show the most primitive characteristics
within the Hominoidea (Fleagle, 1984). This view is supported by results from comparative
studies of a wide array of morphological (Biegert, 1973; Remane, 1921; Sawalischin,
1911; Schultz, 1933, 1973; Wislocki, 1929, 1932), physiological (Hellekant et al.,
1990), cytogenetic (Wienberg & Stanyon, 1987) and molecular data (Darga et al.,
1973, 1984; Dene et al., 1976; Doolittle et al., 1971; Felsenstein, 1987; Goldman
et al., 1987; Sarich & Cronin, 1976; Sibley & Ahlquist, 1984, 1987).

Figure 1. Systematic position
of the gibbons within the primate order.

There is considerably less agreement on the phylogenetic
relationships among gibbon species; some views are shown in Fig. 2. Several authors
suggest that among modern gibbons, the siamang (S. syndactylus) was the first
species to split off from the main stem (Bruce & Ayala, 1979; Creel & Preuschoft,
1976, 1984). Others disagree and see the crested gibbons (concolor group)
in that position (Groves, 1972; Haimoff, 1983; Haimoff et al., 1982, 1984), and according
to a third view the siamang and the crested gibbons share a common ancestor not shared
by other gibbons (Shafer, 1986; van Tuinen & Ledbetter, 1983, 1989). Apparently,
the "relationships of the main divisions are very even, and any dichotomy is
hard to elucidate" (Groves, 1989).

There is some agreement to the extent that the genus
Hylobates can be divided into four systematic groups which are summarised
in Table 1. The four groups have been recognised as subgenera (i.e. Hylobates,
Bunopithecus, Nomascus, and Symphalangus, respectively) for
several years (e.g. Geissmann, 1995a; Marshall & Sugardjito, 1986; Prouty et
al., 1983). The participants of a Workshop on Primate Taxonomy (held in Orlando, Forida, Feb. 2000)
proposed to elevate these subgenera to genus rank. This recommendation is followed
here. Each of the four genera is, among other characteristics, identified by a distinctive
karyotype; they differ in the diploid number of chromosomes, as shown in Table 1.
More recently, this classification received strong support from a comparative analysis
of DNA sequences (Roos & Geissmann, 2001).

As shown by Mootnick and Groves (2005), the earlier
genus name Bunopithecus is not applicable to hoolock gibbons, because the
type specimen of Bunopithecus - a fossil mandibular fragment from a Mid-Pleistocene
fissure deposit in Sichuan province, China - is outside the range of modern Hylobatidae
in its dental characters. Therefore, the authors supplied the new generic name Hoolock
for hoolock gibbons.

Within the 44-chromosome gibbons (genus Hylobates),
Kloss's gibbon (H. klossii) has for some time been considered to be the first
species to have differentiated from the main stock (Chivers, 1977; Creel & Preuschoft,
1976, 1984; Groves, 1989; Haimoff, 1983; Haimoff et al., 1982, 1984). The remaining
group of gibbons has been referred to as the lar group (Brockelman & Gittins,
1984; Groves, 1972, 1984; Haimoff et al., 1984; Marshall & Sugardjito, 1986;
Marshall et al., 1984). According to more recent studies on gibbon vocalisations
(Geissmann, 1993, 2002a, 2002b) and mitochondrial DNA sequences (Garza & Woodruff,
1992), the traditional exclusion of Kloss's gibbon from the lar group may
not be justified. On the other hand, a closer affinity between Kloss's gibbon and
the crested gibbons (genus Nomascus), as suggested by Berger and Tylinek (1984,
p. 174), is not supported by current data.

3. Adopting a Systematic
Framework

In order to discuss the phylogenetic relationships
within any group of animals, it is necessary to define clearly the various taxa under
comparison at the outset. Therefore, the purpose of this chapter is to review briefly
the current status of gibbon classification at the species level. The classification
adopted here will serve as a provisional working base for the chapters to follow.

During the last 30 years, several reviews of gibbon
taxonomy have been published (Chivers, 1977; Chivers & Gittins, 1978; Groves,
1972, 1984, 1993; Marshall & Sugardjito, 1986; Napier & Napier, 1967). New
evidence on gibbon systematics became available in such a steady stream that each
review was in need of revision only a few years after its publication - and this
will without doubt happen to the present publication.

Although still frequently cited, the gibbon taxonomy
used by Napier and Napier (1967) has become outdated today because of a considerable
amount of new information published after the release of this important textbook.
Groves' monograph (1972) not only contains a useful review of the literature on gibbon
taxonomy published before 1970, but to this day also remains the most impressive
compilation and review of data relating to the topic, including the most comprehensive
survey of museum specimens. Chivers (1977), Chivers and Gittins (1978) and Groves
(1984, 1993) presented modifications and additions to the taxonomy proposed by Groves
(1972). These changes mainly resulted from the increasing knowledge gained from various
field studies.

Marshall and Sugardjito (1986) combined data from
their own studies on both wild gibbons and museum specimens. Their first-hand knowledge
of song- and fur-characteristics of many gibbon populations, together with detailed
distribution maps, colour illustrations of the subspecies within the lar group,
and a review of the recent literature, makes this probably the single most recommendable
introduction to gibbon classification at this time. With only few modifications,
this paper will be used here as the standard reference for the taxonomy of the lesser
apes.

The major modification concerns the crested gibbons
(concolor group): Whereas Marshall and Sugardjito (1986) recognised only one
species (namely N. concolor), four species are recognised here. Recognition
of the light-cheeked gibbon (N. leucogenys) as a separate species from the
black crested gibbon (N. concolor) was proposed mainly because of anatomical
differences between the two taxa - especially in the size of the penis bone (baculum)
(Dao Van Tien, 1983; Ma & Wang, 1986). In addition, evidence from museum specimens
appeared to suggest that areas of sympatry between the forms exist both in China
and in Vietnam (Dao Van Tien, 1983; Ma & Wang, 1986), although my own examination
of the same museum material did not support this conclusion (Geissmann, unpublished
data).

A suggested species-level differentiation between
N. leucogenys and N. gabriellae was also based on differences in the
penis bone (Groves, 1993; Groves & Wang, 1990); however, only one such bone has
been studied of N. gabriellae. Own studies on large samples demonstrate that
all three forms (concolor, leucogenys and gabriellae) differ
markedly in their song (Geissmann, 1993, 1995a; Geissmann et al., 2000).

A further form, siki, whose distribution
area is situated between that of N. gabriellae and N. leucogenys, has
previously been identified as a subspecies N. gabriellae by Groves (Groves,
1993; Groves & Wang, 1990), based on a penis bone at the Muséum National
d'Histoire Naturelle in Paris. Unfortunately, this particular bone is not suitable
to determine the affinities of siki, because it is (1) incomplete and (2)
not of siki but of N. leucogenys (Geissmann, unpublished data). On
the other hand, the song of zoo speciemns of siki, although having distinct
characteristics, resembles that of N. leucogenys more than that of any other
form of crested gibbon including N. gabriellae (Geissmann, unpublished data).
Likewise, mitochondrial DNA sequences suggest that siki is more closely related
to leucogenys than to gabriellae (Garza & Woodruff, 1992, 1994).
As additional evidence for a close relationship between leucogenys and siki,
it should also been noted that the females of both forms are so similar in fur colouration
that no distinctive features are known, at present, whereas both differ from females
of N. gabriellae (Geissmann, 1995a; Geissmann et al., 2000). Here, siki
is recognised as a full species, following Groves (2001).

Ma and Wang (1986) described the subspecies N.
concolor furvogaster from western Yunnan province (China). I consider recognition
of this subspecies highly questionable. Own studies using all museum specimens of
this form demonstrated that its distinguishing characteristics are based on the description
of subadult females which have not attained their adult colouration. Adult females
of "furvogaster" do not exhibit these characteristics but resemble
females of N. c. concolor and females from central Yunnan which have been
described as N. c. jingdongensis (Ma & Wang, 1986). Whether or not the
latter form deserves separation from N. c. concolor is also debatable.

Own studies demonstrate that vocalisations of black
crested gibbons from Cao Bang province in northeastern Vietnam and adjacent Guangxi
province (China) resemble songs of N. hainanus from the island of Hainan,
but both differ radically from songs of all other crested gibbons. These eastern
black crested gibbons were provisionally referred to as N. sp. cf. nasutus
(Geissmann, 1997, 2002b, Geissmann et al., 2000, and unpublished data; see also Geissmann,
1989). As it has become clear more recently that the Hainan and the mainland populations
strongly differ in fur colouration (Geissmann, unpublished data), both populations
should be recognized as full species. These are N. nasutus from the mainland
and N. hainanus from Hainan.

Within the lar group, there is some controversy
about the phylogenetic affinities of the Bornean race albibarbis (Groves,
1984): Whereas vocal characteristics of this gibbon are virtually identical to those
of H. agilis, its fur colouration shows some similarities to H. muelleri
muelleri, which also occurs in Borneo. Both forms share a common border of distribution
along the Barito River in Southwest Borneo, and both hybridise at the headwaters
of the Barito River (Brockelman & Gittins, 1984; Marshall & Sugardjito, 1986;
Marshall et al., 1984; Mather, 1992). As a result, the options for the systematic
treatment of albibarbis include, among others, making it a subspecies of either
H. agilis or H. muelleri, separating albibarbis as yet another
species, or combining H. agilis, H. muelleri and albibarbis
into one species (Groves, 1984). In the present study, albibarbis is recognised
as a full species, following Groves (2001).

For most gibbon taxa, several different vernacular
names are in use. There are no international guidelines for the creation of such
names, but the inconsistency of their use, the inaccuracy or ambiguity of their meaning
can sometimes be misleading. In Figure 3 and in the Gallery pages, the
most frequently used vernacular names are provided for each species. The classification
of the genus Hylobates used here is summarised in Table 2.

Table 2. Classification of the Hylobatidae (showing
scientific and English names).

Table 2. Classification and distribution of gibbon subspecies. (Questionable
subspecies are identified with a question mark.)

Table 2. Subspecies and distribution of the genus Hylobates.
(Questionable subspecies are identified with a question mark.)

Species

Subspecies

Distribution

Common name

Hoolock1

H. hoolock

Assam, Bangladesh, Burma west of Chindwin river

Western hoolock gibbon

H. leuconedys

Burma east of Chindwin river, west Yunnan (China)

Eastern hoolock gibbon

Hylobates

H. agilis

agilis

West Sumatra (Indonesia)

Mountain agile gibbon

?unko 2

Malay peninsula, east Sumatra (Indonesia)

Lowland agile gibbon

H. albibarbis

Southwest Borneo between Kapuas and Barito river (Indonesia)

White-bearded gibbon

H. klossii

Mentawai Islands (Indonesia)

Kloss's or Mentawai gibbon

H. lar 3

lar

Malay peninsula

Malaysian lar or white-handed gibbon

carpenteri

North Thailand, east Burma, west Laos

Carpenter's lar or white-handed gibbon

entelloides 4

Central and south Thailand, southeast Burma

Central lar or white-handed gibbon

vestitus

North Sumatra (Indonesia)

Sumatran lar or white-handed gibbon

?yunnanensis 5

Southwest Yunnan (China)

Yunnan lar or white-handed gibbon

H. moloch

moloch

West Java (Indonesia)

Western silvery or Western Javan gibbon

? pongoalsoni 6

Central Java (Indonesia)

Eastern silvery or Central Javan gibbon

H. muelleri

muelleri

Southeast Borneo east of Barito river (Indonesia)

Southern or Muller's gray gibbon

abbotti

West Borneo north of Kapuas river (Indonesia)

Abbott's gray gibbon

funereus

North Borneo (Indonesia, Malaysia, Brunei)

Northern gray gibbon

? new ssp.

Central east Borneo (Indonesia)

-

H. pileatus

East Thailand, west Cambodia

Pileated or capped gibbon

Nomascus

N. concolor

concolor

North Vietnam, central Yunnan (China) between Black
and Red rivers

Tonkin black crested gibbon

?furvogaster 7

West Yunnan, between Salween and Mekong river

West Yunnan black crested gibbon

?jingdongensis 7

Central Yunnan, between Mekong and Black river

Jingdong black crested gibbon

?lu 7

Bokeo Province (northwest Laos)

Laotian black crested gibbon

N. hainanus

Hainan Island (China)

Hainan crested gibbon

N. nasutus

Northeast Vietnam, east of Red River

Cao-vit crested gibbon

N. leucogenys

North Laos, northwest Vietnam, south Yunnan (China)

Northern white-cheeked crested gibbon

N. siki

South Laos, central Vietnam

Southern white-cheeked crested gibbon

N. gabriellae

South Laos, south Vietnam, east Cambodia

Yellow-cheeked crested gibbon

Symphalangus

S. syndactylus

syndactylus

Sumatra (Indonesia)

Sumatran siamang

?continentis 8

Malay peninsula

Malaysian siamang

1
The earlier genus name Bunopithecus is not applicable to hoolock gibbons,
because the type specimen of Bunopithecus (a fossil mandibular fragment from
a Mid-Pleistocene fissure deposit in Sichuan province, China) is outside the range
of modern Hylobatidae in its dental characters (Mootnick and Groves, 2005).2
Differs from H. a. agilis in the higher frequency of darker color morphs and
the lower frequency of the lighter morphs. This distinction does not permit an identification
of individuals of unknown provenience. Additional research necessary.3
Research necessary to distinguish features of various subspecies.4
Elevated body weights at isthmus of Kra may indicate additional taxon (Geissmann,
unpublished data).5
Very similar to, and possibly synonymous with, H. l. carpenteri.6
Based only on preliminary molecular data (Andayani et al., 1998, 2001).7
Very similar to, and possibly synonymous with, N. c. concolor.8
May be slightly smaller than Sumatran form based on dental measurements; no body
weights of wild animals are available from the Malayan peninsula and no other distinguishing
characteristics are known.

4. Gibbon Distribution

The gibbons are distributed throughout the tropical
rain forests of Southeast Asia (e.g. Chivers, 1977; Groves, 1972; Marshall &
Sugardjito, 1986). A distribution map of the main systematic divisions (i.e. the
genera) of the Hylobatidae is shown in Figure 4. In order to keep this map and the
following maps simple, the distribution areas are mostly depicted like large continuous
areas, which they probably were in the origin. Mainly as a result of habitat destruction,
present distribution areas are considerably more fragmented than indicated in these
figures, often consisting of isolated and (sometimes very small) patches of more
or less virginal forest. Maps of the remaining areas of the tropical forests in Asia
are shown in Collins et al. (1991).

Gibbon species are almost everywhere separated by
rivers and straits. The only extensive degree of sympatry is between the siamang
(genus Symphalangus) and the lar group (genus Hylobates) and
was probably made possible by the strong size difference between them: Over the whole
range of its distribution, the siamang occurs in sympatry with either H. agilis
or H. lar. A small area of sympatry may have existed between the genus Nomascus
(N. concolor) and the genus Hylobates (H. lar) in southwestern
Yunnan (see Figure 4) (Ma & Wang, 1986; Zhang et al., 1992).

The species distribution for the genus Hoolock
is shown in Figure 5, that for the genus Hylobates is shown in Figure 6.

Figure 5. Distribution of the species of the genus Hoolock.

Figure 6. Distribution of
the species of the genus Hylobates (References: Chivers & Gittins, 1978;
Geissmann, 1991; Ma & Wang, 1986; Marshall & Sugardjito, 1986). Nos. 1-3
refer to areas of sympatry and hybridisation which are described in the text.

Within the genus Hylobates, three areas of
sympatry with some hybridisation are known. They are numbered in Figure 6 as follows:

1) H. lar and H. pileatus at the headwaters of the Takhon River in
Khao Yai National Park, about 120 km NE of Bangkok (Thailand). As late as 1925, sympatry
between these two species apparently also extended to about 80 km SE of Bangkok (Geissmann,
1991), but gibbon habitat now appears to have been destroyed in most parts of this
zone. The area of overlap in the Khao Yai National Park is about 100 km2,
where hybrids constitute about 5% of the breeding population (Brockelman & Gittins,
1984; Marshall & Sugardjito, 1986; Marshall & Brockelman, 1986).

2) H. agilis and H. lar at the headwaters of the Muda River in the
north-western part of Peninsular Malaysia. A small number of mixed groups and hybrids
have been found there on the shores of a artificial lake (Brockelman & Gittins,
1984; Gittins, 1978).

3) H. albibarbis and H. muelleri at the headwaters of the Barito River
in Kalimantan (Brockelman & Gittins, 1984; Marshall & Sugardjito, 1986).
This area is particularly interesting: A zone of at least 3,500 km2
is inhabited by an apparently stable hybrid population (Mather, 1992). No pure-species
individuals have been found in the area, suggesting that gene flow from the adjacent
pure populations into the area must be very limited.

The approximate subspecies distriution for the white-handed
gibbon (Hylobates lar) is shown in Figure 7.

Figure 7. Approximate distribution
of the subspecies of the white-handed gibbon (Hylobates lar).

Contact zones between species of the concolor
group are less well known. Small areas of sympatry have been reported to occur between
N. concolor and N. leucogenys in southern Yunnan (China) and northern
Vietnam (Dao Van Tien, 1983; Ma & Wang, 1986). A possible wild-born hybrid between
these two species has been described by Geissmann (1995b). A contact zone of unknown
extent, possibly with some hybridisation, may occur between the respective distribution
areas of N. gabriellae and N. siki in southern Vietnam and Laos (see
Fig. 6), but not much data on that zone is available. Groves (1972) regards museum
specimens from Saravane (Laos) as intergrades between gabriellae and siki.
Gibbon songs from Xe Piane (southern Laos) appear to be intermediates between gabriellae
and siki. Gibbon songs from the Bolovens Plateau (southern Laos, NE of Xe
Piane) and from Bach Ma (central Vietnam) sound like siki, but Museum specimens
from the same localities (American Museum of Natural History, New York, and Naturhistoriska
Riksmuseet, Stockholm, respectively) clearly look like gabriellae. A recent
review of museum skins and tape-recordings of wild gibbons suggests that a very large
zone with gibbons of unknown identity exists which may be an intergrade zone between
siki and gabriellae, or which may be inhabited by gibbons of an as
yet undiscribed taxon (Geissmann et al., 2000).

While Chinese gibbons today are restricted to southern
Yunnan and Hainan (Fooden et al., 1987; Geissmann, 1989; Groves & Wang, 1990;
Ma & Wang, 1986), their former distribution range extended as far north as the
Yellow River in historical times (Gao et al., 1981; van Gulik, 1967; Zhang et al.,
1992), as shown in Figure 9. The identity of these gibbons is unclear. Although the
more southern populations were, in all probability, members of the genus Nomascus,
Pleistocene fossils (mainly confined to individual teeth) from the more northern
part of this now gibbon-less area have been referred to both Nomascus and
Hoolock (Groves, 1972; Gu, 1989; Marshall & Sugardjito, 1986). Several
old Chinese paintings of gibbons are reproduced in Van Gulik (1967). At least the
most naturalistic of these paintings strikingly resembles Hoolock hoolock.
It is attributed to Yi Yuanji (ca 1000-1064 AD), who reportedly had wandered
all over south Hubei and north Hunan Provinces in order to observe wild gibbons.